Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T03:16:03.789Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluation of different culture systems with low oxygen tension on the development, quality and oxidative stress-related genes of bovine embryos produced in vitro

Published online by Cambridge University Press:  24 March 2011

Maria Elena Arias ,
Raul Sanchez  and
Ricardo Felmer
Maria Elena Arias
Affiliation:
Laboratorio de Biotecnología Animal, Instituto de Investigaciones Agropecuarias, INIA-Carillanca, Temuco, Chile. Centro de Biotecnología de la Reproducción. Universidad de La Frontera, Temuco, Chile.
Raul Sanchez
Affiliation:
Centro de Biotecnología de la Reproducción. Universidad de La Frontera, Temuco, Chile.
Ricardo Felmer*
Affiliation:
Laboratorio de Biotecnología Animal, Instituto de Investigaciones Agropecuarias, INIA-Carillanca. Camino Cajon Vilcun s/n Km. 10. Casilla 58-D, Temuco, Chile.
*
All correspondence to: Ricardo Felmer. Laboratorio de Biotecnología Animal, Instituto de Investigaciones Agropecuarias, INIA-Carillanca. Camino Cajon Vilcun s/n Km. 10. Casilla 58-D, Temuco, Chile. Tel: +56 45 215706. Fax: +56 45 216112. e-mail: rfelmer@inia.cl
Get access Rights & Permissions [Opens in a new window]

Summary

The present study was conducted to assess the development, quality and gene expression profile of oxidative stress-related genes of bovine embryos cultured in different culture systems with low oxygen tension (5% CO2, 5% O2 and 90% N2). The systems assessed included: (1) an incubator chamber; (2) a plastic bag; and (3) a foil bag. The choice of culture system had no effect on cleavage rate at 72 h. However, significant differences (P < 0.01) were observed in the rate of blastocysts registered at day 7 (29.8, 20.2 and 12.7% for incubator chamber, plastic bag and foil bag, respectively). Total number of cells did not differ between systems, although the proportion of ICM:total cells was affected particularly in the plastic bag (19.5%), compared with the incubator chamber (31.4%). In addition, significant differences were found in the apoptotic:total cell ratio (3.3, 6.5 and 8.8% for the incubator chamber, plastic bag and foil bag, respectively), with apoptotic nuclei localised mainly in the ICM compartment of the embryo. The amount of reactive oxygen species was also different between culture systems and this effect was correlated with a higher expression of SOD2, GSS and GPX1 genes in embryos cultured in the gassed bags as compared with embryos cultured in the incubator chamber. In conclusion, these results give evidence that, under low oxygen tension, the incubator chamber is more efficient and generates higher number of, and better quality, embryos than gassed bag systems evaluated here and this effect was probably due to an increased level of reactive oxygen species in the gassed bags, which upregulates the expression of some antioxidant enzymes to compensate for hyperoxia conditions.

Keywords

Bovine embryosGassed bagsGene expressionOxygen tension
Type
Research Article
Information
Zygote , Volume 20 , Issue 3 , August 2012 , pp. 209 - 217
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adam, A.A., Takahashi, Y., Katagiri, S. & Nagano, M. (2004). Effects of oxygen tension in the gas atmosphere during in vitro maturation, in vitro fertilization and in vitro culture on the efficiency of in vitro production of mouse embryos. Jpn J. Vet. Res. 52, 77–84.Google ScholarPubMed
Byrne, A.T., Southgate, J., Brison, D.R. & Leese, H.J. (1999). Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J. Reprod. Fertil. 117, 97–105.CrossRefGoogle ScholarPubMed
Correa, G.A., Rumpf, R., Mundim, T.C., Franco, M.M. & Dode, M.A. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–142.CrossRefGoogle ScholarPubMed
El Mouatassim, S., Guerin, P. & Menezo, Y. (1999). Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Mol. Hum. Reprod. 5, 720–725.CrossRefGoogle ScholarPubMed
Farin, P.W. & Farin, C.E. (1995). Transfer of bovine embryos produced in vivo or in vitro: survival and fetal development. Biol. Reprod. 52, 676–682.CrossRefGoogle ScholarPubMed
Farin, P.W., Crosier, A.E. & Farin, C.E. (2001). Influence of in vitro systems on embryo survival and fetal development in cattle. Theriogenology 55, 151–170.CrossRefGoogle ScholarPubMed
Fischer, B. & Bavister, B.D. (1993). Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J. Reprod. Fertil. 99, 673–679.CrossRefGoogle ScholarPubMed
Fouladi-Nashta, A.A., Alberio, R., Kafi, M., Nicholas, B., Campbell, K.H. & Webb, R. (2005). Differential staining combined with TUNEL labelling to detect apoptosis in preimplantation bovine embryos. Reprod. Biomed. Online 10, 497–502.CrossRefGoogle ScholarPubMed
Fukui, Y., McGowan, L.T., James, R.W., Pugh, P.A. & Tervit, H.R. (1991). Factors affecting the in-vitro development to blastocysts of bovine oocytes matured and fertilized in vitro. J. Reprod. Fertil. 92, 125–131.CrossRefGoogle ScholarPubMed
Gardner, R.L. (1989). Cellular basis of morphogenesis. CIBA Found. Symp. 144, 172–181.Google Scholar
Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A. & Peelman, L.J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5, 27.CrossRefGoogle ScholarPubMed
Goto, Y., Noda, Y., Mori, T. & Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic. Biol. Med. 15, 69–75.CrossRefGoogle ScholarPubMed
Guerin, P., El Mouatassim, S. & Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.CrossRefGoogle ScholarPubMed
Hagemann, L.J., Weilert, L.L., Beaumont, S.E. & Tervit, H.R. (1998). Development of bovine embryos in single in vitro production (sIVP) systems. Mol. Reprod. Dev. 51, 143–147.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Hardy, K. (1999). Apoptosis in the human embryo. Rev. Reprod. 4, 125–134.CrossRefGoogle Scholar
Hardy, K., Handyside, A.H. & Winston, R.M. (1989). The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development 107, 597–604.CrossRefGoogle ScholarPubMed
Hasler, J.F. (2000). In vitro culture of bovine embryos in Menezo's B2 medium with or without coculture and serum: the normalcy of pregnancies and calves resulting from transferred embryos. Anim. Reprod. Sci. 60–61, 81–91.CrossRefGoogle ScholarPubMed
Iwasaki, S. & Nakahara, T. (1990). Incidence of embryos with chromosomal anomalies in the inner cell mass among bovine blastocysts fertilized in vitro. Theriogenology 34, 683–690.CrossRefGoogle ScholarPubMed
Johnson, M.H. & Nasr-Esfahani, M.H. (1994). Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Bioessays 16, 31–38.CrossRefGoogle ScholarPubMed
Kitagawa, Y., Suzuki, K., Yoneda, A. & Watanabe, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62, 1186–1197.CrossRefGoogle ScholarPubMed
Koo, D.B., Kang, Y.K., Choi, Y.H., Park, J.S., Kim, H.N., Oh, K.B., Son, D.S., Park, H., Lee, K.K. & Han, Y.M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol. Reprod. 67, 487–492.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25, 402–408.CrossRefGoogle Scholar
Lonergan, P., Rizos, D., Kanka, J., Nemcova, L., Mbaye, A.M., Kingston, M., Wade, M., Duffy, P. & Boland, M.P. (2003). Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction 126, 337–346.CrossRefGoogle ScholarPubMed
Moss, J.I., Pontes, E. & Hansen, P.J. (2009). Insulin-like growth factor-1 protects preimplantation embryos from anti-developmental actions of menadione. Arch. Toxicol. 83, 1001–1007.CrossRefGoogle ScholarPubMed
Mundim, T.C., Ramos, A.F., Sartori, R., Dode, M.A., Melo, E.O., Gomes, L.F., Rumpf, R. & Franco, M.M. (2009). Changes in gene expression profiles of bovine embryos produced in vitro, by natural ovulation, or hormonal superstimulation. Genet. Mol. Res. 8, 1398–1407.CrossRefGoogle ScholarPubMed
Nagao, Y., Saeki, K., Hoshi, M. & Kainuma, H. (1994). Effects of oxygen concentration and oviductal epithelial tissue on the development of in vitro matured and fertilized bovine oocytes cultured in protein-free medium. Theriogenology 41, 681–687.CrossRefGoogle ScholarPubMed
Orsi, N.M. & Leese, H.J. (2001). Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol. Reprod. Dev. 59, 44–53.CrossRefGoogle ScholarPubMed
Palma, G., Olivier, N., Alberio, R. & Brem, G. (1998). In vitro development and viability of bovine embryos produced without gassed incubator. Theriogenology 49, 213.CrossRefGoogle Scholar
Parrish, J.J., Susko-Parrish, J.L., Leibfried-Rutledge, M.L., Critser, E.S., Eyestone, W.H. & First, N.L. (1986). Bovine in vitro fertilization with frozen–thawed semen. Theriogenology 25, 591–600.CrossRefGoogle ScholarPubMed
Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.CrossRefGoogle Scholar
Remacle, J., Lambert, D., Raes, M., Pigeolet, E., Michiels, C. & Toussaint, O. (1992). Importance of various antioxidant enzymes for cell stability. Confrontation between theoretical and experimental data. Biochem. J. 286 (Pt 1), 41–46.CrossRefGoogle ScholarPubMed
Rinaudo, P.F., Giritharan, G., Talbi, S., Dobson, A.T. & Schultz, R.M. (2006). Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil. Steril. 86, 1252–1265.CrossRefGoogle ScholarPubMed
Rodriguez, K.F. & Farin, C.E. (2004). Gene transcription and regulation of oocyte maturation. Reprod. Fertil. Dev. 16, 55–67.CrossRefGoogle ScholarPubMed
Salas-Vidal, E., Lomeli, H., Castro-Obregon, S., Cuervo, R., Escalante-Alcalde, D. & Covarrubias, L. (1998). Reactive oxygen species participate in the control of mouse embryonic cell death. Exp. Cell Res. 238, 136–147.CrossRefGoogle ScholarPubMed
Suzuki, T., Sumantri, C., Khan, N.H., Murakami, M. & Saha, S. (1999). Development of a simple, portable carbon dioxide incubator for in vitro production of bovine embryos. Anim. Reprod. Sci. 54, 149–157.CrossRefGoogle ScholarPubMed
Tam, P.P. (1988). The allocation of cells in the presomitic mesoderm during somite segmentation in the mouse embryo. Development 103, 379–390.CrossRefGoogle ScholarPubMed
Tarin, J.J. (1996). Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol. Hum. Reprod. 2, 717–724.CrossRefGoogle ScholarPubMed
Thompson, J.G. (2000). In vitro culture and embryo metabolism of cattle and sheep embryos–a decade of achievement. Anim. Reprod. Sci. 60–61, 263–275.CrossRefGoogle ScholarPubMed
Vajta, G., Holm, P., Greve, T. & Callesen, H. (1997). The submarine incubation system, a new tool for in vitro embryo culture: a technique report. Theriogenology 48, 1379–1385.CrossRefGoogle Scholar
Van Soom, A., Yuan, Y.Q., Peelman, L.J., de Matos, D.G., Dewulf, J., Laevens, H. & de Kruif, A. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology 57, 1453–1465.CrossRefGoogle ScholarPubMed
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A. Jr., Sirisathien, S., Brackett, B. & Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16, 893–901.CrossRefGoogle ScholarPubMed
Yuan, Y.Q., Van Soom, A., Coopman, F.O., Mintiens, K., Boerjan, M.L., Van Zeveren, A., de Kruif, A. & Peelman, L.J. (2003). Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 59, 1585–1596.CrossRefGoogle ScholarPubMed